Developmental life history is associated with variation in rates of climatic niche evolution in a salamander adaptive radiation*

Rates of climatic niche evolution vary widely across the tree of life and are strongly associated with rates of diversification among clades. However, why the climatic niche evolves more rapidly in some clades than others remains unclear. Variation in life history traits often plays a key role in determining the environmental conditions under which species can survive, and therefore, could impact the rate at which lineages can expand in available climatic niche space. Here, we explore the relationships among life-history variation, climatic niche breadth, and rates of climatic niche evolution. We reconstruct a phylogeny for the genus Desmognathus, an adaptive radiation of salamanders distributed across eastern North America, based on nuclear and mitochondrial genes. Using this phylogeny, we estimate rates of climatic niche evolution for species with long, short, and no aquatic larval stage. Rates of climatic niche evolution are unrelated to the mean climatic niche breadth of species with different life histories. Instead, we find that the evolution of a short larval period promotes greater exploration of climatic space, leading to increased rates of climatic niche evolution across species having this trait. We propose that morphological and physiological differences associated with variation in larval stage length underlie the heterogeneous ability of lineages to explore climatic niche space. Rapid rates of climatic niche evolution among species with short larval periods were an important dimension of the clade's adaptive radiation and likely contributed to the rapid rate of lineage accumulation following the evolution of an aquatic life history in this clade. Our results show how variation in a key life-history trait can constrain or promote divergence of the climatic niche, leading to variation in rates of climatic niche evolution among species.     

Evolution of the climatic niche in scaly tree ferns (Cyatheaceae,Polypodiopsida)

Although climatic niche conservatism has been assumed by a large number of studies focused on climatic niche evolution, there are examples of climatic niche diversification and adaptation to changing climates. In this article, we reconstruct a climatic niche of scaly tree ferns (Cyatheaceae) using a rigorous analytical procedure which combines climatic niche modelling with reconstruction of continuous characters given a phylogenetic hypothesis. To estimate the limits to climatic niches of species, we used climate envelope modelling and ordination. Ancestral climatic niches of species were reconstructed by maximum likelihood and least‐squares analyses. We observed a trend towards niche conservatism with occasional events of niche transformations in scaly tree ferns. We discuss the implications of our study with respect to the potential and limitations for applications of niche modelling to evolutionary studies. We suggest that future studies of evolution of climatic niches could be considerably improved by employing approaches enabling reconstruction of continuous response to climatic gradients. Further progress may also be achieved by exploring models of character evolution other than the Brownian motion model. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 165 , 1–19.     

The evolution of climate tolerance in conifer‐feeding aphids in relation to their host's climatic niche

Climate adaptation has major consequences in the evolution and ecology of all living organisms. Though phytophagous insects are an important component of Earth's biodiversity, there are few studies investigating the evolution of their climatic preferences. This lack of research is probably because their evolutionary ecology is thought to be primarily driven by their interactions with their host plants. Here, we use a robust phylogenetic framework and species‐level distribution data for the conifer‐feeding aphid genus Cinara to investigate the role of climatic adaptation in the diversity and distribution patterns of these host‐specialized insects. Insect climate niches were reconstructed at a macroevolutionary scale, highlighting that climate niche tolerance is evolutionarily labile, with closely related species exhibiting strong climatic disparities. This result may suggest repeated climate niche differentiation during the evolutionary diversification of Cinara. Alternatively, it may merely reflect the use of host plants that occur in disparate climatic zones, and thus, in reality the aphid species' fundamental climate niches may actually be similar but broad. Comparisons of the aphids' current climate niches with those of their hosts show that most Cinara species occupy the full range of the climatic tolerance exhibited by their set of host plants, corroborating the hypothesis that the observed disparity in Cinara species' climate niches can simply mirror that of their hosts. However, 29% of the studied species only occupy a subset of their hosts' climatic zone, suggesting that some aphid species do indeed have their own climatic limitations. Our results suggest that in host‐specialized phytophagous insects, host associations cannot always adequately describe insect niches and abiotic factors must be taken into account.     

Climate niche conservatism does not explain restricted distribution patterns in Tynanthus (Bignonieae,Bignoniaceae)

Studies on niche evolution allow us to establish how species niches have changed over time and to identify how long‐term evolutionary processes have led to present‐day species distributions. Here, we investigate the patterns of climatic niche evolution in Tynanthus (Bignonieae, Bignoniaceae), a genus of narrowly distributed species. We test the hypothesis that niche conservatism has played an important role in the history of this group of Neotropical lianas. We perform univariate and multivariate comparisons between climatic niches of species and associated environmental data with information on phylogenetic relationships. We encountered considerable divergence in niches among species, indicating that niche conservatism in climatic variables does not seem to have played a key role in the history of the genus. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 95–109.     

OAK CATKINS,LEAVES AND FRUITS FROM THE OLIGOCENE CATAHOULA FORMATION AND THEIR EVOLUTIONARY SIGNIFICANCE

Remains of staminate inflorescences, leaves, and fruits of Quercus from the Oligocene Catahoula Formation show striking similarity to modern subgenera Erythrobalanus (catkins and leaves) and Lepidobalanus (fruits). The appearance of modern subgenera in the Oligocene, only a short period of time after the first occurrences of Quercus in the fossil, record suggest a period of rapid evolution resulting in the modernization of Quercus. It is suggested that this period of relatively rapid evolution was in response to global climatic changes initiated at the Eocene-Oligocene boundary that may have been exaggerated by an Oligocene global lowstand of sea level. The climatic deterioration induced by these events may have allowed Paleogene Quercus to enter new adaptive zones through migration and hybridization culminating in the final major modernization of the oaks.     

Niche conservatism and phylogenetic clustering in a tribe of arid‐adapted marsupial mice,the Sminthopsini

The progressive expansion of the Australian arid zone during the last 20 Ma appears to have spurred the diversification of several families of plants, vertebrates and invertebrates, yet such taxonomic groups appear to show limited niche radiation. Here, we test whether speciation is associated with niche conservatism (constraints on ecological divergence) or niche divergence in a tribe of marsupial mice (Sminthopsini; 23 taxa) that includes the most speciose genus of living dasyurids, the sminthopsins. To that end, we integrated phylogenetic data with ecological niche modelling, to enable us to reconstruct the evolution of climatic suitability within Sminthopsini. Niche overlap among species was low‐moderate (but generally higher than expected given environmental background similarity), and the degree of phylogenetic clustering increased with aridity. Climatic niche reconstruction illustrates that there has been little apparent evolution of climatic tolerance within clades. Accordingly, climatic disparity tends to be accumulated among clades, suggesting considerable niche conservatism. Our results also indicate that evolution of climatic tolerances has been heterogeneous across different dimensions of climate (temperature vs. precipitation) and across phylogenetic clusters (Sminthopsis murina group vs. other groups). Although some results point to the existence of shifts in climatic niches during the speciation of sminthopsins, our study provides evidence for substantial phylogenetic niche conservatism in the group. We conclude that niche diversification had a low impact on the speciation of this tribe of small, but highly mobile marsupials.     

Phylogeny and biogeography of the American live oaks (Quercus subsection Virentes): a genomic and population genetics approach

The nature and timing of evolution of niche differentiation among closely related species remains an important question in ecology and evolution. The American live oak clade, Virentes, which spans the unglaciated temperate and tropical regions of North America and Mesoamerica, provides an instructive system in which to examine speciation and niche evolution. We generated a fossil‐calibrated phylogeny of Virentes using RADseq data to estimate divergence times and used nuclear microsatellites, chloroplast sequences and an intron region of nitrate reductase (NIA‐i3) to examine genetic diversity within species, rates of gene flow among species and ancestral population size of disjunct sister species. Transitions in functional and morphological traits associated with ecological and climatic niche axes were examined across the phylogeny. We found the Virentes to be monophyletic with three subclades, including a southwest clade, a southeastern US clade and a Central American/Cuban clade. Despite high leaf morphological variation within species and transpecific chloroplast haplotypes, RADseq and nuclear SSR data showed genetic coherence of species. We estimated a crown date for Virentes of 11 Ma and implicated the formation of the Sea of Cortés in a speciation event ~5 Ma. Tree height at maturity, associated with fire tolerance, differs among the sympatric species, while freezing tolerance appears to have diverged repeatedly across the tropical–temperate divide. Sympatric species thus show evidence of ecological niche differentiation but share climatic niches, while allopatric and parapatric species conserve ecological niches, but diverge in climatic niches. The mode of speciation and/or degree of co‐occurrence may thus influence which niche axis plants diverge along.     

Ecogeographical differentiation patterns inAdonis sect.Consiligo (Ranunculaceae)

Adonis sect.Consiligo is split into three subsections based on morphology, growth pattern, pollen and fruit morphology. For all species distribution maps are provided and discussed with regard to their ecology and climatic requirements. These data reveal additional characters that support the classification of the taxa. Most species of the section grow in continental Eurasiatic steppes and mountain steppe habitats. Only the species of subsect.Amurenses grow in Far Eastern temperate forests and prefer a more oceanic climate. The taxonomic position of these strongly divergent species is supported by the distributional and ecological data. The evolution ofAdonis sect.Consiligo occurred under strong climatic control. During evolution the taxa could only slightly widen their ecological amplitude and, thus, ecology remained rather stable except that of the subsect.Amurenses. Ecological and distributional data can be used to validate taxonomy and phylogeny and reveal additional informations.     

Defining climate's role in ecosystem evolution: Clues from late quaternary mammals

Mammalian communities alter their taxonomic composition through time as the species composing them change their biogeographic range, become extinct, or evolve into new species. When taxonomic compositions change through these processes, inevitably the links between taxa and communities change too, resulting in evolution from one ecosystem into the next. Late Quaternary examples suggest that on a timescale encompassing a few thousand to a few hundred thousand years (the “multi‐millennial timescale"), climatic change is perhaps the most important driver of ecosystem evolution because it periodically forces biogeographic changes and extinction. Climatic change over this timescale, which essentially slips between “geological time”; and “ecological time”;, is not very closely in phase with population‐level evolution of a species analyzed for this study, the meadow vole Microtus pennsylvanicus; therefore climatic oscillations on the multi‐millennial timescale may not stimulate speciation much. Instead, speciation may contribute to ecosystem evolution independent of climatic change and over a longer time scale.     

Heat freezes niche evolution

Climate change is altering phenology and distributions of many species and further changes are projected. Can species physiologically adapt to climate warming? We analyse thermal tolerances of a large number of terrestrial ectotherm (n = 697), endotherm (n = 227) and plant (n = 1816) species worldwide, and show that tolerance to heat is largely conserved across lineages, while tolerance to cold varies between and within species. This pattern, previously documented for ectotherms, is apparent for this group and for endotherms and plants, challenging the longstanding view that physiological tolerances of species change continuously across climatic gradients. An alternative view is proposed in which the thermal component of climatic niches would overlap across species more than expected. We argue that hard physiological boundaries exist that constrain evolution of tolerances of terrestrial organisms to high temperatures. In contrast, evolution of tolerances to cold should be more frequent. One consequence of conservatism of upper thermal tolerances is that estimated niches for cold‐adapted species will tend to underestimate their upper thermal limits, thereby potentially inflating assessments of risk from climate change. In contrast, species whose climatic preferences are close to their upper thermal limits will unlikely evolve physiological tolerances to increased heat, thereby being predictably more affected by warming.     

Rapid adaptive evolution of the diapause program during range expansion of an invasive mosquito

In temperate climates, the recurring seasonal exigencies of winter represent a fundamental physiological challenge for a wide range of organisms. In response, many temperate insects enter diapause, an alternative developmental program, including developmental arrest, that allows organisms to synchronize their life cycle with seasonal environmental variation. Geographic variation in diapause phenology contributing to local climatic adaptation is well documented. However, few studies have examined how the rapid evolution of a suite of traits expressed across the diapause program may contribute to climatic adaptation on a contemporary timescale. Here, we investigate the evolution of the diapause program over the past 35 years by leveraging a “natural experiment” presented by the recent invasion of the Asian tiger mosquito, Aedes albopictus, across the eastern United States. We sampled populations from two distinct climatic regions separated by 6° of latitude (∼700 km). Using common-garden experiments, we identified regional genetic divergence in diapause-associated cold tolerance, diapause duration, and postdiapause starvation tolerance. We also found regional divergence in nondiapause thermal performance. In contrast, we observed minimal regional divergence in nondiapause larval growth traits and at neutral molecular marker loci. Our results demonstrate rapid evolution of the diapause program and imply strong selection caused by differences in winter conditions.     

Mammal diversity and environment evolution during the Plio-Pleistocene in East Africa

Human evolution began in East Africa four million years ago, with a transition from an arboreal state to a more terrestrial one. This evolution seems to be correlated with a large environmental change in East Africa around 2.5 m.y. due to a major climatic change leading to drier and cooler conditions. Cenogram analysis (a graphical representation of community structure) can be used to reconstruct the vegetation cover at a regional scale, and to infer the changing climatic conditions. Using cenogram sequences of different sites along the Rift Valley, we were able to determine the regional ecological context in which mammals and hominids have evolved in East Africa during the last 3 million years. Between 3.5 and 2 m.y., during a general climatic change, successive faunas of South Tanzania reflect the progressive opening of their environment. In contrast around Lake Turkana a mosaic of isolated dry and wet habitats were present throughout this period. At this time, the Rift seems to have been spatially structured in several basins isolated from one other, and isolated faunas experienced separate speciation events (particularly with the appearance ofHomo genus). After 2 m.y., the disappearance of the isolating barriers on one hand, and a regional increase in aridity, on the other hand, led to more homogenous faunas arising throughout the region. Replacements of mammal species occurred (especiallyHomo erectus replacingHomo habilis) and several others mammal species, including australopithecines, disappeared during this same period.     

The niches of nuthatches affect their lineage evolution differently across latitude

Ecological niche evolution can promote or hinder the differentiation of taxa and determine their distribution. Niche‐mediated evolution may differ among climatic regimes, and thus, species that occur across a wide latitudinal range offer a chance to test these heterogeneous evolutionary processes. In this study, we examine (a) how many lineages have evolved across the continent‐wide range of the Eurasian nuthatch (Sitta europaea), (b) whether the lineages’ niches are significantly divergent or conserved and (c) how their niche evolution explains their geographic distribution. Phylogenetic reconstruction and ecological niche models (ENMs) showed that the Eurasian nuthatch contained six parapatric lineages that diverged within 2 Myr and did not share identical climatic niches. However, the niche discrepancy between these distinct lineages was relatively conserved compared with the environmental differences between their ranges and thus was unlikely to drive lineage divergence. The ENMs of southern lineages tended to cross‐predict with their neighbouring lineages whereas those of northern lineages generally matched with their abutting ranges. The coalescence‐based analyses revealed more stable populations for the southern lineages than the northern ones during the last glaciation cycle. In contrast to the overlapping ENMs, the smaller parapatric distribution suggests that the southern lineages might have experienced competitive exclusion to prevent them from becoming sympatric. On the other hand, the northern lineages have expanded their ranges and their current abutting distribution might have resulted from lineages adapting to different climatic conditions in allopatry. This study suggests that niche evolution may affect lineage distribution in different ways across latitude.     

Tectonics,climate and the diversification of the tropical African terrestrial flora and fauna

Tropical Africa is home to an astonishing biodiversity occurring in a variety of ecosystems. Past climatic change and geological events have impacted the evolution and diversification of this biodiversity. During the last two decades, around 90 dated molecular phylogenies of different clades across animals and plants have been published leading to an increased understanding of the diversification and speciation processes generating tropical African biodiversity. In parallel, extended geological and palaeoclimatic records together with detailed numerical simulations have refined our understanding of past geological and climatic changes in Africa. To date, these important advances have not been reviewed within a common framework. Here, we critically review and synthesize African climate, tectonics and terrestrial biodiversity evolution throughout the Cenozoic to the mid-Pleistocene, drawing on recent advances in Earth and life sciences. We first review six major geo-climatic periods defining tropical African biodiversity diversification by synthesizing 89 dated molecular phylogeny studies. Two major geo-climatic factors impacting the diversification of the sub-Saharan biota are highlighted. First, Africa underwent numerous climatic fluctuations at ancient and more recent timescales, with tectonic, greenhouse gas, and orbital forcing stimulating diversification. Second, increased aridification since the Late Eocene led to important extinction events, but also provided unique diversification opportunities shaping the current tropical African biodiversity landscape. We then review diversification studies of tropical terrestrial animal and plant clades and discuss three major models of speciation: (i) geographic speciation via vicariance (allopatry); (ii) ecological speciation impacted by climate and geological changes, and (iii) genomic speciation via genome duplication. Geographic speciation has been the most widely documented to date and is a common speciation model across tropical Africa. We conclude with four important challenges faced by tropical African biodiversity research: (i) to increase knowledge by gathering basic and fundamental biodiversity information; (ii) to improve modelling of African geophysical evolution throughout the Cenozoic via better constraints and downscaling approaches; (iii) to increase the precision of phylogenetic reconstruction and molecular dating of tropical African clades by using next generation sequencing approaches together with better fossil calibrations; (iv) finally, as done here, to integrate data better from Earth and life sciences by focusing on the interdisciplinary study of the evolution of tropical African biodiversity in a wider geodiversity context.     

ASYNCHRONOUS EVOLUTION OF PHYSIOLOGY AND MORPHOLOGY IN ANOLIS LIZARDS

Species‐rich adaptive radiations typically diversify along several distinct ecological axes, each characterized by morphological, physiological, and behavioral adaptations. We test here whether different types of adaptive traits share similar patterns of evolution within a radiation by investigating patterns of evolution of morphological traits associated with microhabitat specialization and of physiological traits associated with thermal biology in Anolis lizards. Previous studies of anoles suggest that close relatives share the same “structural niche” (i.e., use the same types of perches) and are similar in body size and shape, but live in different “climatic niches” (i.e., use habitats with different insolation and temperature profiles). Because morphology is closely tied to structural niche and field active body temperatures are tied to climatic niches in Anolis, we expected phylogenetic analyses to show that morphology is more evolutionarily conservative than thermal physiology. In support of this hypothesis, we find (1) that thermal biology exhibits more divergence among recently diverged Anolis taxa than does morphology; and (2) diversification of thermal biology among all species often follows diversification in morphology. These conclusions are remarkably consistent with predictions made by anole biologists in the 1960s and 1970s.     

Brain size diversity in adaptation and speciation of subterranean mole rats

We have tested brain size diversity and encephalization in the actively speciating subterranean mole rats of the Spalax ehrenbergi superspecies in Israel. Our sample involved 171 individuals comprising 12 populations and 4 chromosomal species (2n = 52, 54, 58 and 60) distributed parapatrically from the northern Mediterranean region southward (2n = 52, 54→+58→60) into increasingly more arid and unpredictable climatic regimes, approaching the Negev Desert. Our results indicate that relative brain size and encephalization are highest in 2n = 60 as compared with 2n = 52, 54 and 58. We hypothesize that this pattern is adaptive and molded by natural selection. Brain evolution and higher encephalization in the S. ehrenbergi complex appears to be associated with increasing ecological stresses of aridity and climatic unpredictability.     

The role of historical factors and natural selection in the evolution of breeding systems of Oxalis alpina in the Sonoran desert ‘Sky Islands’

Pleistocene climatic oscillations are known to influence the patterns of genetic diversity and the distribution of traits that are the target of selection. Here, we combine phylogeographical and ecological niche modelling (ENM) approaches to explore the influence of historical factors (Pleistocene climatic shifts) and natural selection on the evolution of distyly (two floral morphs) from tristyly (three floral morphs) of Oxalis alpina in the Sky Islands of the Sonoran Desert. Molecular data and ENM indicate that historical factors have had a strong influence on the genetic structure and the geographical distribution of reproductive systems of O. alpina. Moreover, genetic results suggest the possibility that distylous populations do not represent a monophyletic group. We propose that the combined effects of natural selection and genetic drift have influenced the tristyly–distyly transition.     

Parallel adaptation to climate above the 35th parallel

Independent or parallel evolution of similar traits is key to understanding the genetics and limitations of adaptation. Adaptation from the same genetic changes in different populations defines parallel evolution. Such genetic changes can derive from standing ancestral variation or de novo mutations and excludes instances of adaptive introgression. In this issue of Molecular Ecology, Walden et al.(2020) investigate the scale of parallel climate adaptation from standing genetic variation between two North American Arabidopsis lyrata lineages, each formed by a distinct evolutionary history during the last glacial cycle. By identifying adaptive variants correlated with three ecologically significant climatic gradients, they show that instead of the same genetic variants or even genes, parallel evolution is only observed at the level of biological processes. The evolution of independent adaptive variants to climate in two genetically close lineages is explained by their different post‐glacial demographic histories. Separate glacial refugia and strong population bottlenecks were probably sufficient to change the landscape of shared allele frequencies, hindering the possibility of parallel evolution.     

HOW IS THE RATE OF CLIMATIC‐NICHE EVOLUTION RELATED TO CLIMATIC‐NICHE BREADTH?

The rate of climatic‐niche evolution is important to many research areas in ecology, evolution, and conservation biology, including responses of species to global climate change, spread of invasive species, speciation, biogeography, and patterns of species richness. Previous studies have implied that clades with higher rates of climatic‐niche evolution among species should have species with narrower niche breadths, but there is also evidence suggesting the opposite pattern. However, the relationships between rate and breadth have not been explicitly analyzed. Here, we examine the relationships between the rate of climatic‐niche evolution and climatic‐niche breadth using phylogenetic and climatic data for 250 species in the salamander family Plethodontidae, a group showing considerable variation in both rates of climatic‐niche evolution and climatic‐niche breadths. Contrary to some expectations, we find no general relationship between climatic‐niche breadth and the rate of climatic‐niche evolution. Climatic‐niche breadths for some ecologically important climatic variables considered separately (temperature seasonality and annual precipitation) do show significant relationships with the rate of climatic‐niche evolution, but rates are faster in clades in which species have broader (not narrower) niche breadths. In summary, our results show that narrower niche breadths are not necessarily associated with faster rates of niche evolution.     

Mitochondrial variation in small brown planthoppers linked to multiple traits and probably reflecting a complex evolutionary trajectory

While it has been proposed in several taxa that the mitochondrial genome is associated with adaptive evolution to different climatic conditions, making links between mitochondrial haplotypes and organismal phenotypes remains a challenge. Mitonuclear discordance occurs in the small brown planthopper (SBPH), Laodelphax striatellus, with one mitochondrial haplogroup (HGI) more common in the cold climate region of China relative to another form (HGII) despite strong nuclear gene flow, providing a promising model to investigate climatic adaptation of mitochondrial genomes. We hypothesized that cold adaptation through HGI may be involved, and considered mitogenome evolution, population genetic analyses, and bioassays to test this hypothesis. In contrast to our hypothesis, chill‐coma recovery tests and population genetic tests of selection both pointed to HGII being involved in cold adaptation. Phylogenetic analyses revealed that HGII is nested within HGI, and has three nonsynonymous changes in ND2, ND5 and CYTB in comparison to HGI. These molecular changes likely increased mtDNA copy number, cold tolerance and fecundity of SBPH, particularly through a function‐altering amino acid change involving M114T in ND2. Nuclear background also influenced fecundity and chill recovery (i.e., mitonuclear epistasis) and protein modelling indicates possible nuclear interactions for the two nonsynonymous changes in ND2 and CYTB. The high occurrence frequency of HGI in the cold climate region of China remains unexplained, but several possible reasons are discussed. Overall, our study points to a link between mtDNA variation and organismal‐level evolution and suggests a possible role of mitonuclear interactions in maintaining mtDNA diversity.